Bering Sea Marine Invasive Species Assessment Alaska Center for Conservation Science
Scientific Name: Petricolaria pholadiformis Phylum Mollusca Common Name false angelwing Class Bivalvia Order Veneroida Family Petricolidae Z:\GAP\NPRB Marine Invasives\NPRB_DB\SppMaps\PETPHO.pn g 164 Final Rank 44.11 Data Deficiency: 8.75
Category Scores and Data Deficiencies Total Data Deficient Category Score Possible Points
Distribution and Habitat: 13.5 26 3.75
Anthropogenic Influence: 4 10 0
Biological Characteristics: 19.5 25 5.00
Impacts: 3.25 30 0 Figure 1. Occurrence records for non-native species, and their geographic proximity to the Bering Sea. Ecoregions are based on the classification system by Spalding et al. (2007). Totals: 40.25 91.25 8.75 Occurrence record data source(s): NEMESIS and NAS databases.
General Biological Information Tolerances and Thresholds Minimum Temperature (°C) 1 Minimum Salinity (ppt) 10
Maximum Temperature (°C) 26 Maximum Salinity (ppt) 35
Minimum Reproductive Temperature (°C) NA Minimum Reproductive Salinity (ppt) 31*
Maximum Reproductive Temperature (°C) NA Maximum Reproductive Salinity (ppt) 35*
Additional Notes
Petricolaria pholadiformis is a bivalve with an elongated white shell. Many lines radiate from the umbo, and the first ten of these are rather well-defined. The shell is also marked by concentric growth lines. Adult shells measure ~55 mm. Adults live burrowed in substrates such as mud, soft rock, or clay. P. pholadiformis is native to eastern North America, and has been introduced to Europe and the western coast of North America. The most likely vectors of introduction for this species are accidental transport with the Eastern oyster (Crassostrea virginica), and transport via ballast water.
Report updated on Wednesday, December 06, 2017 Page 1 of 13 1. Distribution and Habitat 1.1 Survival requirements - Water temperature
Choice: Little overlap – A small area (<25%) of the Bering Sea has temperatures suitable for year-round survival Score: C 1.25 of High uncertainty? 3.75 Ranking Rationale: Background Information: Temperatures required for year-round survival occur in a limited This species has been reported from Penobscot Bay, ME where water area (<25%) of the Bering Sea. Thresholds are based on geographic temperatures range from 1.1 to 14.1°C (NERACOOS 2016). In its distribution, which may not represent physiological tolerances; we native range, this species occurs as far south as Padre Island, TX (in the therefore ranked this question with "High uncertainty". Gulf of Mexico), where water temperatures >26°C have been recorded (NOAA 2017).
Sources: NERACOOS 2016 NOAA 2017
1.2 Survival requirements - Water salinity
Choice: Considerable overlap – A large area (>75%) of the Bering Sea has salinities suitable for year-round survival Score: A 3.75 of 3.75
Ranking Rationale: Background Information: Salinities required for year-round survival occur over a large Based on its geographic distribution, this species can tolerate salinities (>75%) area of the Bering Sea. up to 35 ppt (Fofonoff et al. 2003). Although it is a marine species, it is usually associated with sites that have some freshwater inflow. Experiments by Castagna and Chalney (1973, qtd. in Fofonoff et al. 2003) found high (90%) survival rates in individuals exposed to 10 ppt water for 52 to 92 days.
Sources: NEMESIS; Fofonoff et al. 2003
1.3 Establishment requirements - Water temperature
Choice: Unknown/Data Deficient Score: U of
Ranking Rationale: Background Information: More information is needed to establish reproductive temperature Duval (1963) observed larvae and spawning at water temperatures requirements for this species. between 16 and 19°C.
Sources: NEMESIS; Fofonoff et al. 2003 Duval 1963
Report updated on Wednesday, December 06, 2017 Page 2 of 13 1.4 Establishment requirements - Water salinity
Choice: Considerable overlap – A large area (>75%) of the Bering Sea has salinities suitable for reproduction Score: A 3.75 of High uncertainty? 3.75 Ranking Rationale: Background Information: Although salinity thresholds are unknown, this species is a marine No information found. organism that does not require freshwater to reproduce. We therefore assume that this species can reproduce in saltwater (31 to 35 ppt). These salinities occur in a large (>75%) portion of the Bering Sea.
Sources: NEMESIS; Fofonoff et al. 2003
1.5 Local ecoregional distribution
Choice: Present in an ecoregion greater than two regions away from the Bering Sea Score: D 1.25 of 5
Ranking Rationale: Background Information: This species is found in southern BC and in WA. On the west coast of North America, this species occurs in WA and southern BC. Individuals have been found in CA, but it is unknown whether there are established populations.
Sources: NEMESIS; Fofonoff et al. 2003
1.6 Global ecoregional distribution
Choice: In few ecoregions globally Score: C 1.75 of 5
Ranking Rationale: Background Information: This species has only been reported from a few ecoregions, mostly This species has a broad native range, from PEI to FL, and west to TX. in northern Europe and in limited areas of western North America. On the west coast of North America, populations are established in WA and BC. In Europe, this species has been found in England, and in the North Sea off the coasts of Belgium, Denmark, and Norway. It is also present in western Sweden. Populations have also been found in Greece, where they were likely introduced by ballast water.
Sources: NEMESIS; Fofonoff et al. 2003
Report updated on Wednesday, December 06, 2017 Page 3 of 13 1.7 Current distribution trends
Choice: Established outside of native range, but no evidence of rapid expansion or long-distance dispersal Score: C 1.75 of 5
Ranking Rationale: Background Information: This species has failed to establish in CA. Introductions have been This species has likely been introduced accidentally with Eastern attributed to transport by anthropogenic vectors, rather than natural oysters, or by ballast water (Fofonoff et al. 2003). Individuals have been dispersal. This species has a restricted worldwide distribution, and found in CA, but do not seem to have established populations there. we have not found evidence of a rapid range expansion for this Zenetos et al. (2009) rejected the possibility that this soecies was species. introduced to the Mediterranean by natural dispersal.
Sources: NEMESIS; Fofonoff et al. 2003 Zenetos et al. 2009
Section Total - Scored Points: 13.5 Section Total - Possible Points: 26.25 Section Total -Data Deficient Points: 3.75
Report updated on Wednesday, December 06, 2017 Page 4 of 13 2. Anthropogenic Transportation and Establishment 2.1 Transport requirements: relies on use of shipping lanes (hull fouling, ballast water), fisheries, recreation, mariculture, etc. for transport
Choice: Has been observed using anthropogenic vectors for transport and transports independent of any anthropogenic vector once Score: A introduced 4 of 4
Ranking Rationale: Background Information: Believed to be transported by hitchhiking or ballast water. Its Introduced outside of its native range by hitchhiking or by ballast water spread in northern Europe has been attributed to natural, larval (Fofonoff et al. 2003). Rosenthal (1980) claims that this species spread dispersal. through northern Europe naturally. In Greece, however, this species has a very disjunct distribution, occurring there and nowhere else along the Mediterranean. For this reason, Zenetos et al. (2009) believe that P. pholadiformis was introduced in Greece by human vectors.
Sources: NEMESIS; Fofonoff et al. 2003 Zenetos et al. 2009 Rosenthal 1980
2.2 Establishment requirements: relies on marine infrastructure, (e.g. harbors, ports) to establish
Choice: Does not use anthropogenic disturbance/infrastructure to establish Score: D 0 of 4
Ranking Rationale: Background Information: This species burrows and establishes in natural substrates. Burrows in natural substrates including mud, peat, clay, and wood (Zenetos et al. 2009).
Sources: Zenetos et al. 2009
2.3 Is this species currently or potentially farmed or otherwise intentionally cultivated?
Choice: No Score: B 0 of 2
Ranking Rationale: Background Information: This species is not farmed or cultivated. Although this species is edible, it is not farmed.
Sources: NEMESIS; Fofonoff et al. 2003
Section Total - Scored Points: 4 Section Total - Possible Points: 10 Section Total -Data Deficient Points: 0
Report updated on Wednesday, December 06, 2017 Page 5 of 13 3. Biological Characteristics 3.1 Dietary specialization
Choice: Generalist at all life stages and/or foods are readily available in the study area Score: A 5 of 5
Ranking Rationale: Background Information: Food items for this species are readily available in the Bering Sea. This species is a filter feeder that consumes phytoplankton and other particles.
Sources: NEMESIS; Fofonoff et al. 2003
3.2 Habitat specialization and water tolerances Does the species use a variety of habitats or tolerate a wide range of temperatures, salinity regimes, dissolved oxygen levels, calcium concentrations, hydrodynamics, pollution, etc?
Choice: Generalist; wide range of habitat tolerances at all life stages Score: A 5 of 5
Ranking Rationale: Background Information: This species can tolerate a range of environmental conditions and This species requires a burrows in moderately soft substrates (e.g., clay, substrate types. mud, chalk, wood) (Tillin and Budd 2008; Zenetos et al. 2009). However, this species is not a boring specialist and cannot burrow into very hard substrates or in soft, loose mud (Tillin and Budd 2008; Jensen 2010). It usually inhabits shallow depths, but has been reported from a range of tidal zones (Tillin and Budd 2008; Zenetos et al. 2009). It is usually associated with sites that receive freshwater input (Zenetos et al. 2009). This species can tolerate a broad range of temperatures and salinities.
Sources: Zenetos et al. 2009 Tillin and Budd 2008 Jensen 2010
3.3 Desiccation tolerance
Choice: Unknown Score: U of
Ranking Rationale: Background Information: The desiccation tolerance of this species is unknown. No information found.
Sources: NEMESIS; Fofonoff et al. 2003
Report updated on Wednesday, December 06, 2017 Page 6 of 13 3.4 Likelihood of success for reproductive strategy i. Asexual or hermaphroditic ii. High fecundity (e.g. >10,000 eggs/kg) iii. Low parental investment and/or external fertilization iv. Short generation time
Choice: Moderate – Exhibits one or two of the above characteristics Score: B 3.25 of 5
Ranking Rationale: Background Information: This species is dioecious and exhibits sexual reproduction, external This species reproduces sexually and exhibits external fertilization. fertilization, and high fecundity. Hermaphoriditism has not been observed (Duval 1963). Fecundity estimates for this species vary widely: ranging from ~ 325 000 to > 3 million eggs (Brousseau 1981, qtd. in Fofonoff et al. 2003; Duval 1963). P. pholadiformis can live up to 10 years, and Duval (1963) estimate they reach sexual maturity at 3 years or later.
Sources: NEMESIS; Fofonoff et al. 2003 Duval 1963
3.5 Likelihood of long-distance dispersal or movements Consider dispersal by more than one method and/or numerous opportunities for long or short distance dispersal e.g. broadcast, float, swim, carried in currents; vs. sessile or sink.
Choice: Disperses long (>10 km) distances Score: A 2.5 of High uncertainty? 2.5 Ranking Rationale: Background Information: Although dispersal distances for this species are unknown, given the This species has a long-lived, planktonic larval stage that can last longevity of the planktonic larval stage, we assume that this species between 10 to 14 days (Duval 1963). Larval dispersal is thought to have is capable of long-distance dispersal under favorable hydrologic contributed to the spread of P. pholadiformis in northern Europe conditions. (Rosenthal 1980).
Sources: Duval 1963 Rosenthal 1980
3.6 Likelihood of dispersal or movement events during multiple life stages i. Can disperse at more than one life stage and/or highly mobile ii. Larval viability window is long (days v. hours) iii. Different modes of dispersal are achieved at different life stages (e.g. unintentional spread of eggs, migration of adults)
Choice: High – Exhibits two or three of the above characteristics Score: A 2.5 of 2.5
Ranking Rationale: Background Information: This species has a long-lived, planktonic larval stage. Larvae and The larval stage is planktonic, and is estimated to last between 10 to 14 eggs can be passively dispersed by water currents. Although adults days (Duval 1963). Adults are largely sessile and burrow in substrates, are sessile, they may be disperse by drifting on wood. including wood; thus, they may be transported by drifting (Zenetos et al. 2009).
Sources: Duval 1963 Zenetos et al. 2009
Report updated on Wednesday, December 06, 2017 Page 7 of 13 3.7 Vulnerability to predators
Choice: Multiple predators present in the Bering Sea or neighboring regions Score: D 1.25 of 5
Ranking Rationale: Background Information: This species is preyed upon by several taxa that occur in the Bering P. pholadiformis can be eaten by crabs, fishes, birds, and fossorial Sea. mammals.
Sources: NEMESIS; Fofonoff et al. 2003
Section Total - Scored Points: 19.5 Section Total - Possible Points: 25 Section Total -Data Deficient Points: 5
Report updated on Wednesday, December 06, 2017 Page 8 of 13 4. Ecological and Socioeconomic Impacts 4.1 Impact on community composition
Choice: No impact Score: D 0 of 2.5
Ranking Rationale: Background Information: No impacts have been reported in its introduced range, and this P. pholadiformis was believed to have replaced the native white species is not expected to impact communities in the Bering Sea. piddock, Barnea candida, in Belgium, but B. candida is now much more abundant in Belgium than P. pholadiformis (Jensen 2010). It has had minimal impacts on the west coast of North America (Fofonoff et al. 2003).
Sources: Jensen 2010 NEMESIS; Fofonoff et al. 2003
4.2 Impact on habitat for other species
Choice: Moderate – Causes or has potential to cause changes to one or more habitats Score: B 1.75 of 2.5
Ranking Rationale: Background Information: This species can alter habitats by burrowing in the substrate. As a result of this species' burrowing activities, Duval (1963) observed semi-permanent mounds of sand that marks the entrance of burrows. Duval (1963) documented tunnel lengths between 2.7 and 14.5 cm deep. The burrows of Pholadidae species increase habitat complexity and, in so doing, increase species' diversity (qtd. in Pinn et al. 2005). Upon an individual's death, the burrows that were created may be used as habitat by other organisms (Fofonoff et al. 2003).
Sources: Duval 1963 NEMESIS; Fofonoff et al. 2003 Pinn et al. 2005
4.3 Impact on ecosystem function and processes
Choice: Limited – Causes or potentially causes changes to food webs and/or ecosystem functions, with limited impact and/or within a very Score: C limited region 0.75 of 2.5 High uncertainty? Ranking Rationale: Background Information: This species' burrowing behavior may increase siltation and erosion A study on the burrowing impacts of other piddocks suggests that rates, especially in soft-bottomed habitats. However, themagnitude piddocks may significantly contribute to erosion, especially in soft of this species' effects on ecosystems is unknown. substrate habitats (Pinn et al. 2005). However, erosion estimates by Pinn et al. (2005) may be overly liberal for P. pholadiformis, because they were based on maximum burrowing depths > 80 cm. In a study on P. pholadiformis, Duval (1963) documented relatively short tunnel lengths between 2.7 and 14.5 cm deep. Through its burrowing activities, this species may also alter ecosystems by increasing siltation (Tillin and Budd 2008).
Sources: Tillin and Budd 2008 Duval 1963 Pinn et al. 2005
Report updated on Wednesday, December 06, 2017 Page 9 of 13 4.4 Impact on high-value, rare, or sensitive species and/or communities
Choice: No impact Score: D 0 of 2.5
Ranking Rationale: Background Information: This species is not expected to impact high-value species in the No impacts have been reported. Bering Sea.
Sources: NEMESIS; Fofonoff et al. 2003
4.5 Introduction of diseases, parasites, or travelers What level of impact could the species' associated diseases, parasites, or travelers have on other species in the assessment area? Is it a host and/or vector for recognized pests or pathogens, particularly other nonnative organisms?)
Choice: No impact Score: D 0 of 2.5
Ranking Rationale: Background Information: This species is not known to transport diseases, parasites, or No impacts have been reported. hitchhikers.
Sources: NEMESIS; Fofonoff et al. 2003
4.6 Level of genetic impact on native species Can this invasive species hybridize with native species?
Choice: No impact Score: D 0 of 2.5
Ranking Rationale: Background Information: This species is not expected to hybridize with native species in the No impacts have been reported. Bering Sea.
Sources: NEMESIS; Fofonoff et al. 2003
4.7 Infrastructure
Choice: No impact Score: D 0 of 3
Ranking Rationale: Background Information: This species is not expected to impact infrastructure in the Bering This species can bore into moderately hard material such as rock, wood, Sea. chalk, and limestone. However, no impacts to infrastructure have been reported.
Sources: NEMESIS; Fofonoff et al. 2003
Report updated on Wednesday, December 06, 2017 Page 10 of 13 4.8 Commercial fisheries and aquaculture
Choice: No impact Score: D 0 of 3
Ranking Rationale: Background Information: This species is not expected to impact commercial fishing in the No impacts have been reported. Bering Sea.
Sources: NEMESIS; Fofonoff et al. 2003
4.9 Subsistence
Choice: No impact Score: D 0 of 3
Ranking Rationale: Background Information: This species is not expected to impact subsistence resources in the No impacts have been reported. Bering Sea.
Sources: NEMESIS; Fofonoff et al. 2003
4.101 Recreation
Choice: No impact Score: D 0 of 3
Ranking Rationale: Background Information: This species is not expected to impact recreational opportunities in No impacts have been reported. the Bering Sea.
Sources: NEMESIS; Fofonoff et al. 2003
4.11 Human health and water quality
Choice: Limited – Has limited potential to pose a threat to human health, with limited impact and/or within a very limited region Score: C 0.75 of 3
Ranking Rationale: Background Information: Cases of PSP and other shellfish syndromes are rare in Alaska. All bivalve species can bioaccumulate toxins in their tissues as a result of consuming toxic dinoflagellates. Consuming raw or cooked bivalves can lead to Paralytic Shellfish Poisoning (PSP), which can cause health issues and even death (NIMPIS 2009).
Sources: NIMPIS 2009
Section Total - Scored Points: 3.25 Section Total - Possible Points: 30 Section Total -Data Deficient Points: 0
Report updated on Wednesday, December 06, 2017 Page 11 of 13 5. Feasibility of prevention, detection and control 5.1 History of management, containment, and eradication
Choice: Attempted; control methods are currently in development/being studied Score: C of
Ranking Rationale: Background Information: No attempts have been made to control or eradicate this species. Ballast water exchange is the method currently used by most ships to This species can be transported by ballast water. Research to reduce reduce the spread of species by ballast water. However, it is considered the spread of species in ballast water in ongoing. a short-term or “stop-gap” option until more effective, technology-based methods become available e.g., ballast water treatment systems (Ruiz and Reid 2007). The treatment of ballast water is an active area of research as vessels are forced to comply with new regulations.
Sources: Ruiz and Reid 2007
5.2 Cost and methods of management, containment, and eradication
Choice: Major short-term and/or moderate long-term investment Score: B of
Ranking Rationale: Background Information: To comply with ballast water regulations, vessels will have to equip The costs associated with purchasing a ballast water treatment system themselves with an onboard ballast water treatment system. These depend on the volume of water that needs to be treated. Systems with a systems represent a major short-term cost for vessel owners (up to pump capacity of 200-250 m³/h can cost from $175,000 to $490,000. $3 million), with additional costs over time to maintain and replace The estimated price for larger systems with a pump capacity of around equipment (e.g. chemicals, filters, UV light bulbs). 2000 m³/h range from $650,000 to nearly $3 million.
Sources: Zagdan 2010
5.3 Regulatory barriers to prevent introductions and transport
Choice: Regulatory oversight and/or trade restrictions Score: C of
Ranking Rationale: Background Information: Alaska does not have state regulations on ballast water management, In the U.S., ballast water management (treatment or exchange) and but two federal regulations (USCG and EPA) require mandatory record-keeping is mandatory and regulated by the USCG, with reporting and ballast water treatment or exchange. additional permitting by the Environmental Protection Agency (EPA). Certain vessels (e.g. small vessels or those traveling within 1 Captain of the Port Zone) are exempt from USCG and EPA regulations.
Alaska does not have a state regulations related to the management of aquatic invasive species in discharged ballast water. It relies on the U.S. Coast Guard (USCG) to enforce national standards. In Alaska, data from 2009-2012 show moderate to high compliance with USCG reporting requirements (Verna et al. 2016).
Sources: CFR 2017 EPA 2013 Verna et al. 2016
Report updated on Wednesday, December 06, 2017 Page 12 of 13 5.4 Presence and frequency of monitoring programs
Choice: No surveillance takes place Score: A of
Ranking Rationale: Background Information: No surveillance is taking place for this species.
Sources: None listed
5.5 Current efforts for outreach and education
Choice: No education or outreach takes place Score: A of
Ranking Rationale: Background Information: No education or outreach efforts are in place for this species.
Sources: None listed
Section Total - Scored Points: Section Total - Possible Points: Section Total -Data Deficient Points:
Report updated on Wednesday, December 06, 2017 Page 13 of 13 Bering Sea Marine Invasive Species Assessment Alaska Center for Conservation Science
Literature Cited for Petricolaria pholadiformis
. NIMPIS. 2009. National Introduced Marine Pest Information System. Available from: http://www.marinepests.gov.au/nimpis
. 33 CFR § 151.2050 Additional requirements - nonindigenous species reduction practices
. Environmental Protection Agency (EPA). 2013. Vessel General Permit for Discharges Incidental to the Normal Operation of Vessels (VGP). Washington, D.C., USA. 194 pp.
. Jensen, K. R. 2010. NOBANIS - Invasive Alien Species Fact Sheet – Mya arenaria. Identification key to marine invasive species in Nordic waters – NOBANIS. Available from: https://www.nobanis.org/globalassets/speciesinfo/m/mya-arenaria/mya-arenaria.pdf Acce
. Fofonoff, P. W., G. M. Ruiz, B. Steves, C. Simkanin, and J. T. Carlton. 2017. National Exotic Marine and Estuarine Species Information System. http://invasions.si.edu/nemesis/. Accessed: 15-Sep-2017.
. NOAA. 2017. Coastal Water Temperature Guide. National Oceanic and Atmospheric Administration. Available online: https://www.nodc.noaa.gov/dsdt/cwtg/cpac.html, Accessed 8-Feb-2017.
. Ruiz, G. M., and D. F. Reid. 2007. Current State of Understanding about the Effectiveness of Ballast Water Exchange (BWE) in Reducing Aquatic Nonindigenous Species (ANS) Introductions to the Great Lakes Basin and Chesapeake Bay, USA: Synthesis and Analysi
. Verna, E. D., Harris, B. P., Holzer, K. K., and M. S. Minton. 2016. Ballast-borne marine invasive species: Exploring the risk to coastal Alaska, USA. Management of Biological Invasions 7(2):199–211. doi: 10.3391/mbi.2016.7.2.08
. Zagdan, T. 2010. Ballast water treatment market remains buoyant. Water and Wastewater International 25:14-16.
. NERACOOS. 2016. Historic average monthly water temperature for Penobscot Bay, Jan to Dec 2016. Northeastern Regional Association of Coastal Ocean Observing Systems. Available from: http://www.neracoos.org/ Accessed 22-Feb-2016.
. NOAA. 2017. Historical data for Station IRDT2 - 8776139 - South Bird Island, TX. National Data Buoy Center, National Weather Service, National Oceanic and Atmospheric Administration. Available from: http://www.ndbc.noaa.gov/ Accessed 22-Feb-2017.
. Zenetos, A., Ovalis, P., and E. Theodorou-Vardala. 2009. The American piddock Petricola pholadiformis Lamarck, 1818 spreading in the Mediterranean Sea. Aquatic Invasions 4(2):385-387.
. Rosenthal, H. 1980. Implications of transplantations to aquaculture and ecosystems. Marine Fisheries Review 42: 1-14.
. Tillin, H. M., and G. Budd. 2008. Ceramium sp. and piddocks on eulittoral fossilised peat. In: Tyler-Walters, H., and K. Hiscock, editors. Marine Life Information Network: Biology and Sensitivity Key Information Reviews. Plymouth, UK. Available from: http
. Jensen, K. R. 2010. NOBANIS – Invasive Alien Species Fact Sheet – Petricolaria pholadiformis. Identification key to marine invasive species in Nordic waters – NOBANIS. Available from: https://www.nobanis.org/marine-identification-key/introduction-to-bival
. Duval, D. M. 1963. The biology of Petricola pholadiformis Lamarck (Lammellibranchiata: Petricolidae). Proceedings of the Malacological Society 35: 89-100.
. Pinn, E. H., Richardson, C. A., Thompson, R. C., and S. J. Hawkins. 2005. Burrow morphology, biometry, age and growth of piddocks (Mollusca: Bivalvia: Pholadidae) on the south coast of England. Marine Biology 147: 943–953. doi.org/10.1007/s00227-005-1582-